Postnatal Coronary Morphogenesis and Growth

  • Robert J. Tomanek
Chapter

Abstract

The early postnatal stage of development is characterized by a rapid growth of the myocardium, which occurs by increases in both cardiomyocyte volume and number. This marked and rapid myocardial growth requires a rapid and substantial expansion of the coronary vasculature. In this regard, it has been documented that in the rat heart, approximately 50 % of the capillary bed present in the adult is formed during the first 3 or 4 weeks of life [1]. Many studies have addressed capillary growth using quantitative methods to assess various capillary parameters. These approaches are explained in the following section.

Keywords

Migration Ischemia Albumin Estrogen Lactate 

Abbreviations

EC

Endothelial cell

FGF

Fibroblast growth factor

LV

Left ventricle

LV

Length density (length/mm3)

NA

Numerical density (number/mm2)

RV

Right ventricle

SV

Surface density (surface area/mm3)

TGF-β

Transforming growth factor β

VEGF

Vascular endothelial factor

VV

Volume density (volume/mm3)

References

  1. 1.
    Rakusan K, Turek Z. Protamine inhibits capillary formation in growing rat hearts. Circ Res. 1985;57:393–8.PubMedCrossRefGoogle Scholar
  2. 2.
    Shipley RA, Shipley LJ, Wearn JT. The capillary supply in normal and hypertrophied hearts of rabbits. J Exp Med. 1937;65:29–42.PubMedCrossRefGoogle Scholar
  3. 3.
    Rakusan K, Poupa O. Changes in the diffusion distance in the rat heart muscle during development. Physiol Bohemoslov. 1963;12:220–7.PubMedGoogle Scholar
  4. 4.
    Roberts J, Wearn J. Quantitative changes in the capillary-muscle relationship in human hearts during normal growth and hypertrophy. Am Heart J. 1941;21:617–33.CrossRefGoogle Scholar
  5. 5.
    Rakusan K, du Mesnil de Rochemont W, Braasch W, Tschopp H, Bing RJ. Capacity of the terminal vascular bed during normal growth, in cardiomegaly, and in cardiac atrophy. Circ Res. 1967;21:209–15.PubMedCrossRefGoogle Scholar
  6. 6.
    Rakusan K, Jel’Inek J, Koreck’Y B, Soukupov’A M, Poupa O. Postnatal development of muscle fibres and capillaries in the rat heart. Physiol Bohemoslov. 1965;14:32–7.PubMedGoogle Scholar
  7. 7.
    Voboril Z, Schiebler TH. Development of blood supply in the rat heart. Z Anat Entwicklungsgesch. 1969;129:24–40.PubMedCrossRefGoogle Scholar
  8. 8.
    Smolich JJ, Berger PJ, Walker AM. Interrelation between ventricular function, myocardial blood flow, and O2 consumption changes at birth in lambs. Am J Physiol. 1996;270:H741–9.PubMedGoogle Scholar
  9. 9.
    Olivetti G, Anversa P, Loud AV. Morphometric study of early postnatal development in the left and right ventricular myocardium of the rat. II. Tissue composition, capillary growth, and sarcoplasmic alterations. Circ Res. 1980;46:503–12.PubMedCrossRefGoogle Scholar
  10. 10.
    Muhlfeld C, Singer D, Engelhardt N, Richter J, Schmiedl A. Electron microscopy and microcalorimetry of the postnatal rat heart (Rattus norvegicus). Comp Biochem Physiol A Mol Integr Physiol. 2005;141:310–8.PubMedCrossRefGoogle Scholar
  11. 11.
    van Groningen JP, Wenink AC, Testers LH. Myocardial capillaries: increase in number by splitting of existing vessels. Anat Embryol (Berl). 1991;184:65–70.CrossRefGoogle Scholar
  12. 12.
    Legato M. Cellular mechanisms of normal growth in the mammalian heat. I. Qualitative and quantitative features of ventricular architecture in the dog from birth to five months of age. Circ Res. 1979;44:250–62.PubMedCrossRefGoogle Scholar
  13. 13.
    Smolich JJ, Walker AM, Campbell GR, Adamson TM. Left and right ventricular myocardial morphometry in fetal, neonatal, and adult sheep. Am J Physiol. 1989;257:H1–9.PubMedGoogle Scholar
  14. 14.
    Mattfeldt T, Mall G. Growth of capillaries and myocardial cells in the normal rat heart. J Mol Cell Cardiol. 1987;19:1237–46.PubMedCrossRefGoogle Scholar
  15. 15.
    Rakusan K, Flanagan MF, Geva T, Southern J, Van Praagh R. Morphometry of human coronary capillaries during normal growth and the effect of age in left ventricular pressure-overload hypertrophy. Circulation. 1992;86:38–46.PubMedCrossRefGoogle Scholar
  16. 16.
    Henquell L, Odoroff CL, Honig CR. Coronary intercapillary ­distance during growth: relation to PtO2 and aerobic capacity. Am J Physiol. 1976;231:1852–9.PubMedGoogle Scholar
  17. 17.
    Korecky B, Hai CM, Rakusan K. Functional capillary density in normal and transplanted rat hearts. Can J Physiol Pharmacol. 1982;60:23–32.PubMedCrossRefGoogle Scholar
  18. 18.
    Steinhausen M, Tillmanns H, Thederan H. Microcirculation of the epimyocardial layer of the heart. I. A method for in vivo observation of the microcirculation of superficial ventricular myocardium of the heart and capillary flow pattern under normal and hypoxic conditions. Pflugers Arch. 1978;378:9–14.PubMedCrossRefGoogle Scholar
  19. 19.
    Eliasen P, Amtorp O. Absence of capillary recruitment during increased coronary blood flow in the working dog heart. Acta Physiol Scand. 1985;124:181–7.PubMedCrossRefGoogle Scholar
  20. 20.
    Rakusan K, Campbell SE. Spatial relationship between cardiac mast cells and coronary capillaries in neonatal rats with cardiomegaly. Can J Physiol Pharmacol. 1991;69:1750–3.PubMedCrossRefGoogle Scholar
  21. 21.
    Kolar F, Papousek F, Pelouch V, Ostadal B, Rakusan K. Pressure overload induced in newborn rats: effects on left ventricular growth, morphology, and function. Pediatr Res. 1998;43:521–6.PubMedCrossRefGoogle Scholar
  22. 22.
    Rakusan K, Cicutti N, Kolar F. Effect of anemia on cardiac function, microvascular structure, and capillary hematocrit in rat hearts. Am J Physiol Heart Circ Physiol. 2001;280:H1407–14.PubMedGoogle Scholar
  23. 23.
    Hort W, Severidt HJ. Capillarization and microscopic changes in the myocardium in congenital heart defects. Virchows Arch Pathol Anat Physiol Klin Med. 1966;341:192–203.PubMedGoogle Scholar
  24. 24.
    Oštádal B, Schiebler T, Rychter Z. Relations between the development of the capillary wall and myoarchitecture of the rat heart. Adv Exp Med Biol. 1975;53:375–88.PubMedGoogle Scholar
  25. 25.
    Lojda Z, Ostadal B, Ruzicova M. Ontogenetic development of membrane-bound proteases and some other enzymes in the endothelial lining of the capillary bed of rat and chicken myocardium. Histochem J. 1985;17:555–7.PubMedCrossRefGoogle Scholar
  26. 26.
    Batra S, Rakusan K. Capillary network geometry during postnatal growth in rat hearts. Am J Physiol. 1992;262:H635–40.PubMedGoogle Scholar
  27. 27.
    Tomanek RJ, Doty MK, Sandra A. Early coronary angiogenesis in response to thyroxine: growth characteristics and upregulation of basic fibroblast growth factor. Circ Res. 1998;82:587–93.PubMedCrossRefGoogle Scholar
  28. 28.
    Tomanek RJ, Haung L, Suvarna PR, O’Brien LC, Ratajska A, Sandra A. Coronary vascularization during development in the rat and its relationship to basic fibroblast growth factor. Cardiovasc Res. 1996;31:Spec No:E116–26.Google Scholar
  29. 29.
    Turek Z, Batra S, Rakusan K. Myocardial oxygenation in immature and adult rats. In: Oxygen transport to tissue XV. New York: Plenum Publishing; 1994. p. 253–8.CrossRefGoogle Scholar
  30. 30.
    Rakusan K, Cicutti N, Flanagan MF. Changes in the microvascular network during cardiac growth, development, and aging. Cell Mol Biol Res. 1994;40:117–22.PubMedGoogle Scholar
  31. 31.
    Tornling G, Unge G, Skoog L, Ljungqvist A, Carlsson S, Adolfsson J. Proliferative activity of myocardial capillary wall cells in dipyridamole–treated rats. Cardiovasc Res. 1978;12:692–5.PubMedCrossRefGoogle Scholar
  32. 32.
    Masuda H, Kawamura K, Nanjo H, Sho E, Komatsu M, Sugiyama T, et al. Ultrastructure of endothelial cells under flow alteration. Microsc Res Tech. 2003;60:2–12.PubMedCrossRefGoogle Scholar
  33. 33.
    Zheng W, Seftor EA, Meininger CJ, Hendrix MJ, Tomanek RJ. Mechanisms of coronary angiogenesis in response to stretch: role of VEGF and TGF-beta. Am J Physiol Heart Circ Physiol. 2001;280:H909–17.PubMedGoogle Scholar
  34. 34.
    Zheng W, Christensen LP, Tomanek RJ. Differential effects of cyclic and static stretch on coronary microvascular endothelial cell receptors and vasculogenic/angiogenic responses. Am J Physiol Heart Circ Physiol. 2008;295:H794–800.PubMedCrossRefGoogle Scholar
  35. 35.
    Kiefer FN, Munk VC, Humar R, Dieterle T, Landmann L, Battegay EJ. A versatile in vitro assay for investigating angiogenesis of the heart. Exp Cell Res. 2004;300:272–82.PubMedCrossRefGoogle Scholar
  36. 36.
    Rakusan K, Sarkar K, Turek Z, Wicker P. Mast cells in the rat heart during normal growth and in cardiac hypertrophy. Circ Res. 1990;66:511–6.PubMedCrossRefGoogle Scholar
  37. 37.
    Levick SP, Melendez GC, Plante E, McLarty JL, Brower GL, Janicki JS. Cardiac mast cells: the centrepiece in adverse myocardial remodelling. Cardiovasc Res. 2011;89(1):12–9.PubMedCrossRefGoogle Scholar
  38. 38.
    Janicki JS, Brower GL, Gardner JD, Forman MF, Stewart Jr JA, Murray DB, et al. Cardiac mast cell regulation of matrix metalloproteinase-related ventricular remodeling in chronic pressure or volume overload. Cardiovasc Res. 2006;69:657–65.PubMedCrossRefGoogle Scholar
  39. 39.
    Tomanek RJ, Sandra A, Zheng W, Brock T, Bjercke RJ, Holifield JS. Vascular endothelial growth factor and basic fibroblast growth factor differentially modulate early postnatal coronary angiogenesis. Circ Res. 2001;88:1135–41.PubMedCrossRefGoogle Scholar
  40. 40.
    Donovan MJ, Lin MI, Wiegn P, Ringstedt T, Kraemer R, Hahn R, et al. Brain derived neurotrophic factor is an endothelial cell survival factor required for intramyocardial vessel stabilization. Development. 2000;127:4531–40.PubMedGoogle Scholar
  41. 41.
    Dbaly J. Postnatal development of coronary arteries in the rat. J Anat Entwickl-Gesch. 1973;141:89–101.CrossRefGoogle Scholar
  42. 42.
    Ito T, Harada K, Tamura M, Takada G. In situ morphometric analysis of the coronary arterial growth in perinatal rats. Early Hum Dev. 1998;52:21–6.PubMedCrossRefGoogle Scholar
  43. 43.
    Neufeld HN, Wagenvoort CA, Edwards JE. Coronary arteries in fetuses, infants, juveniles, and young adults. Lab Invest. 1962;11:837–44.PubMedGoogle Scholar
  44. 44.
    Reinecke P, Hort W. [The growth of coronary artery branches in man under physiological conditions. Morphological studies of corrosion casts of the anterior interventricular branch of the coronary artery]. Z Kardiol. 1992;81:110–5.PubMedGoogle Scholar
  45. 45.
    Yasuoka K, Harada K, Tamura M, Takada G. Left anterior descending coronary artery flow and its relation to age in children. J Am Soc Echocardiogr. 2002;15:69–75.PubMedCrossRefGoogle Scholar
  46. 46.
    Dolezel S, Gerova M, Hartmannova B, Vasku J. Development of the adrenergic innervation in the myocardium and coronary arteries of the dog. Acta Anat (Basel). 1990;139:191–200.CrossRefGoogle Scholar
  47. 47.
    Kralios FA, Cluff N, Anderson FL, Hanson GR, Kralios AC. Postnatal development of peptidergic innervation of the canine heart. J Mol Cell Cardiol. 1999;31:215–25.PubMedCrossRefGoogle Scholar
  48. 48.
    Davies H. Atherogenesis and the coronary arteries of childhood. Int J Cardiol. 1990;28:283–91.PubMedCrossRefGoogle Scholar
  49. 49.
    Vlodaver Z, Neufeld HN. The musculo-elastic layer in the coronary arteries. A histological and hemodynamic concept. Vasc Dis. 1967;4:136–45.PubMedGoogle Scholar
  50. 50.
    Moon HD. Coronary arteries in fetuses, infants, and juveniles. Circulation. 1957;16:263–7.PubMedCrossRefGoogle Scholar
  51. 51.
    Vlodaver Z, Abramovici A, Neufeld HN, Liban E. Coronary arteries in Yemenites. J Atheroscler Res. 1967;7:161–70.PubMedCrossRefGoogle Scholar
  52. 52.
    Rapola J, Pesonen E. Coronary artery changes in newborn babies. A histological and electron microscopical study. Acta Pathol Microbiol Scand A. 1977;85:286–96.PubMedGoogle Scholar
  53. 53.
    Moon HD, Rinehart JF. Histogenesis of coronary arteriosclerosis. Circulation. 1952;6:481–8.PubMedCrossRefGoogle Scholar
  54. 54.
    Wilens SL. The nature of diffuse intimal thickening of arteries. Am J Pathol. 1951;27:825–39.PubMedGoogle Scholar
  55. 55.
    Fangman RJ, Hellwig CA. Histology of coronary arteries in newborn infants. Am J Pathol. 1947;23:901.PubMedGoogle Scholar
  56. 56.
    Milei J, Grana DR, Navari C, Azzato F, Guerri-Guttenberg RA, Ambrosio G. Coronary intimal thickening in newborn babies and <or=1-year-old infants. Angiology. 2010;61:350–6.PubMedCrossRefGoogle Scholar
  57. 57.
    Leistikow EA, Bolande RP. Perinatal origins of coronary atherosclerosis. Pediatr Dev Pathol. 1999;2:3–10.PubMedCrossRefGoogle Scholar
  58. 58.
    Kurosawa S, Kurosawa H, Becker AE. The coronary arterioles in newborns, infants and children. A morphometric study of normal hearts and hearts with aortic atresia and complete transposition. Int J Cardiol. 1986;10:43–56.PubMedCrossRefGoogle Scholar
  59. 59.
    Wiest G, Gharehbaghi H, Amann K, Simon T, Mattfeldt T, Mall G. Physiological growth of arteries in the rat heart parallels the growth of capillaries, but not of myocytes. J Mol Cell Cardiol. 1992;24:1423–31.PubMedCrossRefGoogle Scholar
  60. 60.
    Ohuchi H, Beighley PE, Dong Y, Zamir M, Ritman EL. Microvascular development in porcine right and left ventricular walls. Pediatr Res. 2007;61:676–80.PubMedCrossRefGoogle Scholar
  61. 61.
    Zamir M. The physics of coronary blood flow. New York: Springer; 2005.Google Scholar
  62. 62.
    Fernandez B, Buehler A, Wolfram S, Kostin S, Espanion G, Franz WM, et al. Transgenic myocardial overexpression of fibroblast growth factor-1 increases coronary artery density and branching. Circ Res. 2000;87:207–13.PubMedCrossRefGoogle Scholar
  63. 63.
    Dedkov EI, Thomas MT, Sonka M, Yang F, Chittenden TW, Rhodes JM, et al. Synectin/syndecan-4 regulate coronary arteriolar growth during development. Dev Dyn. 2007;236:2004–10.PubMedCrossRefGoogle Scholar
  64. 64.
    Baba F, Swartz K, van Buren R, Eickhoff J, Zhang Y, Wolberg W, et al. Syndecan-1 and syndecan-4 are overexpressed in an estrogen receptor-negative, highly proliferative breast carcinoma subtype. Breast Cancer Res Treat. 2006;98:91–8.PubMedCrossRefGoogle Scholar
  65. 65.
    Fisher DJ, Heymann MA, Rudolph AM. Regional myocardial blood flow and oxygen delivery in fetal, newborn, and adult sheep. Am J Physiol. 1982;243:H729–31.PubMedGoogle Scholar
  66. 66.
    Lopaschuk GD, Collins-Nakai RL, Itoi T. Developmental changes in energy substrate use by the heart. Cardiovasc Res. 1992;26:1172–80.PubMedCrossRefGoogle Scholar
  67. 67.
    Jarmakani JM, Nagatomo T, Nakazawa M, Langer GA. Effect of hypoxia on myocardial high-energy phosphates in the neonatal mammalian heart. Am J Physiol. 1978;235:H475–81.PubMedGoogle Scholar
  68. 68.
    Portman MA, Heineman FW, Balaban RS. Developmental changes in the relation between phosphate metabolites and oxygen consumption in the sheep heart in vivo. J Clin Invest. 1989;83:456–64.PubMedCrossRefGoogle Scholar
  69. 69.
    Portman MA, Ning XH. Myocardial energy metabolism in the newborn lamb in vivo during pacing-induced changes in oxygen ­consumption. Pediatr Res. 1995;37:182–8.PubMedCrossRefGoogle Scholar
  70. 70.
    Yamamoto H, Avkiran M. Left ventricular pressure overload during postnatal development. Effects on coronary vasodilator reserve and tolerance to hypothermic global ischemia. J Thorac Cardiovasc Surg. 1993;105:120–31.PubMedGoogle Scholar
  71. 71.
    Oskarsson G, Pesonen E. Coronary blood flow in healthy neonates: effects of left ventricular function and mass. Pediatr Cardiol. 2004;25:11–6.PubMedCrossRefGoogle Scholar
  72. 72.
    Kozak-Barany A, Jokinen E, Rantonen T, Saraste M, Tuominen J, Jalonen J, et al. Efficiency of left ventricular diastolic function increases in healthy full-term infants during the first months of life. A prospective follow-up study. Early Hum Dev. 2000;57:49–59.PubMedCrossRefGoogle Scholar
  73. 73.
    Flanagan MF, Fujii AM, Colan SD, Flanagan RG, Lock JE. Myocardial angiogenesis and coronary perfusion in left ventricular pressure-overload hypertrophy in the young lamb. Evidence for inhibition with chronic protamine administration. Circ Res. 1991;68:1458–70.PubMedCrossRefGoogle Scholar
  74. 74.
    Flanagan MF, Aoyagi T, Currier JJ, Colan SD, Fujii AM. Effect of young age on coronary adaptations to left ventricular pressure overload hypertrophy in sheep. J Am Coll Cardiol. 1994;24:1786–96.PubMedCrossRefGoogle Scholar
  75. 75.
    Laurie W, Woods JD. Anastomosis in the coronary circulation. Lancet. 1958;2:812–6.PubMedCrossRefGoogle Scholar
  76. 76.
    Reiner L, Vrbanovic D, Madrazo A. Interarterial coronary anastomoses in neonatal pigs. Proc Soc Exp Biol Med. 1961;106:732–4.PubMedGoogle Scholar
  77. 77.
    Schaper W. Collateral circulation: past and present. Basic Res Cardiol. 2009;104:5–21.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Robert J. Tomanek
    • 1
  1. 1.Carver College of Medicine Cardiovascular CenterUniversity of IowaIowa CityUSA

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